Biological cycle of two outstanding nudibranchs from Antarctica

Manuel Ballesteros

Emeritus Professor, Universitat de Barcelona, Facultat de Biologia
Avda. Diagonal, 643, 08028 Barcelona, Spain
Email: mballesteros@ub.edu

Introduction

Nudibranchs living in the ocean surrounding Antarctica have been of interest to naturalists and scientists since the first oceanographic surveys of the Antarctic seabed in the 19th and early 20th centuries. Among the scientific expeditions that describe nudibranch species, it is worth mentioning those of the Challenger (Bergh, 1884), the Scottish National Antarctic Expedition (Eliot, 1905, 1909), the Charcot’s Antarctic Expedition (Vayssière, 1906), the Swedish Antarctic Expedition (Odhner, 1926), the British Antarctic “Terra Nova” Expedition (Odhner, 1934), the University Chile Expedition (Marcus, 1959) and the Expeditions Antarctiques Françaises en Terre Adélie (Vicente & Arnaud, 1974) among others.

In recent decades, and due to numerous research campaigns and the establishment of permanent or seasonal scientific bases, a great interest has been awakened in the investigation of Antarctic marine biodiversity (De Broyer et al., 2014; Rauschert & Arntz, 2015). Regarding nudibranch molluscs, Minichev (1972) studied the nudibranch fauna of the Davis Sea, in remote eastern Antarctica; Cattaneo-Vietti (1991) the nudibranchs of the Ross Sea; Kiko et al. (2008) have studied some aspects of the biology and geographical distribution of Tergipes antarcticus, the only known nudibranch that develops its entire cycle in the lower layer of the Antarctic ice pack. Valdés et al. (2012) have studied the anatomy of some small species of aeolidacean nudibranchs, while Moles et al. (2016) have recently studied the Antarctic species of Doto, describing a new species. Wägele is the one who has distinguished herself in recent decades in the study of the geographical distribution of amtarctic nudibranchs (1987), on Tritoniella belli (1989a), on the genus Bathydoris (1089b), on the species of Notaeolidia (1990a), on the species of the genus Austrodoris (1990b) and on those of the genus Tritonia (1995). Moles et al. (2017) have recently studied the giant eggs of Bathydoris hodgsoni and the embryonic development of this species and of Doris kerguelenensis. In an still unpublished study on sea slugs in the Southern Ocean, a total of 39 species of nudibranchs are reported in Antarctic waters (Ballesteros pers. com.)

This article discusses some morphological and biological aspects of two species of nudibranchs that stand out in the Antarctic benthos: Doris kerguelenensis and Bathydoris hodgsoni, and provides specific data on the different phases of their biological cycle.

 

Materials and Methods

The specimens examined in this study were collected during research expeditions aboard the Spanish research vessel B.I.O. Hespérides (2003) in the Bellingshausen Sea, the German research vessel R.V. Polarstern (2003-2004) in the Weddell Sea, and during scuba diving campaigns on King George Island (South Shetland Islands) as part of the BENTART 2006 campaign.

Photographic documentation of the animals and their spawn masses was carried out using a Konica Minolta Dynax 7D DSLR camera for laboratory specimens and an Olympus SP350 camera housed in a waterproof case for underwater photography.

 

Doris kerguelenensis (Bergh, 1884)

Doris kerguelenensis (formerly classified within the genus Austrodoris) is a widely distributed Antarctic nudibranch, inhabiting the upper infralittoral zone to depths exceeding 1,500 meters (Plate 1). Adult specimens can reach lengths of over 10 cm. The body is typically whitish, although cream or yellowish individuals are not uncommon. Both the rhinophores and gill leaves share the same coloration as the body. The entire mantle is covered in semi-spherical tubercles of varying sizes. This species feeds on a diverse range of sponges, including demosponges such as Dendrilla, Haliclona, Isodictya, and Sphaerotylus, as well as hexactinellids like Rosella and Anoxycalyx (MacDonald & Nybakken, 1997).

Wägele (1990) reviewed the type specimens of Austrodoris species, synonymizing several with D. kerguelenensis. García et al. (1993) conducted a taxonomic and anatomical study of D. kerguelenensis specimens collected from the Scotia Sea during the ANTÁRTIDA 8611 expedition. Various molecules, including the diterpenoid palmadorine and several sesquiterpenoids, have been identified in the mantle of juvenile and adult individuals. The role of these compounds in the animal’s defense mechanism remains unclear (Moles et al., 2017; Avila, 2020).

Originally described from the Kerguelen Islands, D. kerguelenensis has been reported from various Antarctic and subantarctic locations, including the South Shetland Islands, South Orkney Islands, Bouvet Island, Heard Island, Macquarie Island, the Falkland Islands, and Chilean and Argentine Patagonia. While numerous synonyms exist for this species (WoRMS, 2024), recent molecular studies by Maroni, Baker et al. (2022) and Maroni et al. (2022) have revealed that D. kerguelenensis is a species complex comprising at least 29 distinct species. The formal descriptions of these newly identified species are currently pending.

Plate 1. Doris kerguelenensis (Bergh, 1884). A. Underwater photograph of a specimen on seaweed Himantothallus grandifolius at King George Island (South Shetland Islands), 10 m depth. B. Underwater photograph of a specimen on a muddy bottom at King George Island (South Shetland Islands), 20 m depth. C. Detail of the anterior region, showing the rhinophores and dorsal tubercles. D, E. Gill leaves. Photos by M. Ballesteros.

 

Biological Cycle of Doris kerguelenensis (Plate 2, Figure 1)

Doris kerguelenensis exhibits direct development, bypassing a pelagic larval stage. Sexually mature individuals lay eggs in a ribbon-like mass, forming an almost complete circle approximately 7 cm in diameter. The ribbon is 28 mm wide, with 22 mm occupied by the eggs and the remaining portion comprising a semi-transparent membrane.The matrix that surrounds the entire egg and the egg capsules are semi-transparent, while the embryos are yellowish, giving this general colour to the egg. There are 13-15 capsules across the width of the ribbon, they are arranged in a single layer and neatly in oblique rows, except at the ends of the ribbon, and there are between 25 and 28 per cm2 of ovigerous ribbon, with a total of about 2,000 capsules in the entire egg mass. The capsules are taller than they are wide, with a quadrangular or slightly rhomboidal base measuring 2 x 2 mm on each side and 3 mm high; the base (the area facing inwards) is flat while the other end, which faces outwards from the band, is rounded.

Embryonic development within the capsules is asynchronous, with embryos at various stages, from the the two-cell phase, others in the 4-cell phase and others in the 8-cell phase or more, and there are empty capsules without embryos. The embryos are cream-colored and enveloped in a potentially nutritive yellowish material. In advanced stages, juvenile individuals can be observed within the capsules, occupying almost the entire capsule, with the mantle with papillae and the foot being visible under binocular microscope. The newly hatched animals move very slowly, measure about 3 mm in length and have developed rhinophores, clearly visible eyes, tubercles on the back and visible mantle spicules; the gill is not yet formed..

Using the Thompson & Jarman (1986) equation, which takes into account the size of the eggs in relation to the water temperature, Moles et al. (2017) estimated that the embryonic development period for this species may last up to a year.

The various stages of the life cycle of this species are illustrated in the figure below:

Plate 2. Life cycle of Doris kerguelenensis. A. Adult specimen from King George Island (South Shetland Islands). B. Egg mass of a specimen from the Weddell Sea. C. Detail of eggs within the egg mass, showing early-stage embryos and more developed juveniles. D. Detail of an egg with a fully developed juvenile ready to hatch. E. Recently hatched juvenile. F. Juvenile individual from King George Island. Photos by M. Ballesteros

Figure 1. Doris kerguelenensis. A. Entire ovigerous ribbon. B. Detail of a longitudinal section of the ovigerous ribbon. C. Detail of ovigerous capsules with embryos at early stages (2, 4, or 8 cells). D. Ovigerous capsules with embryos in juvenile form. E. Recently hatched juvenile, with a detail of dorsal tubercles and mantle spicules. Original illustrations by M. Ballesteros.

 

Bathydoris hodgsoni Eliot, 1907

The genus Bathydoris comprises seven valid species (WoRMS, 2024), inhabiting cold, deep-water environments. In the Antarctic, only B. hodgsoni and Prodoris clavigera have been reported, with the latter previously classified within the genus Bathydoris due to its morphological similarity.

B. hodgsoni is a large nudibranch, reaching up to 20 cm in length, and exhibits a circumpolar Antarctic distribution. Its coloration varies from dirty white to brown or reddish, especially in larger individuals (Plate 3). A distinctive feature of this species is the numerous pear-shaped, pointed protuberances that cover its dorsal surface. These protuberances are easily dislodged, often resulting in specimens with a nearly bare back, particularly those collected by trawl nets.

The mantle of B. hodgsoni contains a bioactive sesquiterpene, hodgsonal, which is believed to be synthesized by the animal itself. This compound is thought to serve as a defense mechanism against predation by Odontaster validus, a common Antarctic starfish predator (Ávila et al., 2000).

Wägele (1989b) conducted a detailed anatomical study of B. hodgsoni, while Moles et al. (2017) investigated the species’ histology and reproductive biology.

Plate 3. Bathydoris hodgsoni Eliot, 1907. A and B. Medium-sized specimen from the Weddell Sea, showing intact mantle protuberances. C. Detail of the gill leaves (indicated by the arrow), with the anal papilla visible behind. D. Large specimen with most of the dorsal protuberances lost. Photos by M. Ballesteros.

 

Biological Cycle of B. hodgsoni (Plate 4, Figure 2)

The biological cycle of B. hodgsoni exhibits remarkable traits, distinguishing it not only from other mollusks but potentially from all marine invertebrates, as noted by Moles et al. (2017):

• Adults can grow to impressive sizes of 16–20 cm and exhibit exceptional longevity comparable to other long-lived mollusks, such as the cephalopod Nautilus (20 years), the land snail Helix pomatia (20 years), and bivalves of the genus Tridacna (up to 100 years). However, the precise lifespan of B. hodgsoni remains undetermined.
• Few spawns have been observed, but they contain some of the largest eggs recorded among marine invertebrates, reaching up to 5 cm. Clutches typically consist of 1–4 eggs, each enclosed in a robust, leathery capsule. The capsules are slightly oval, with a flattened base and a rounded apex.
• Within each capsule, the embryo undergoes direct development, transforming into a juvenile without passing through a free-swimming veliger larval stage.
• Artificially hatched juveniles measure approximately 3 cm in length. They are creamy white with translucent greenish viscera visible dorsally, likely corresponding to the digestive gland. The right rhinophore is smooth, whitish, and digitate in form. The body and mantle edge, including the anterior and posterior margins, are covered in papillae of varying shapes and sizes. The papillae are semi-transparent with opaque tips, and their surfaces are irregular, marked by small warts. Large papillae may be conical or broad-based, while smaller ones are conical. The central dorsal region lacks large papillae, likely due to detachment, leaving smaller conical papillae in their place. Below the integument, an irregular whitish reticulum is visible, containing groups of white granules that are most abundant dorsally. At the posterior end of the dorsum, 6–7 small gill leaves form a rosette-like circle devoid of papillae. Within this circle, the anal papilla is located slightly off-center, raised, and characterized by a wrinkled anal opening. The foot is whitish with a visible reticulum, similar to the body. The anterior edge is furrowed, and the mouth forms a prominent protuberance anteriorly.
• The development period within the capsule is extraordinarily protracted. Using the equation provided by Thompson & Jarman (1986), which correlates egg size with water temperature, Moles et al. (2017) estimate an embryonic development duration of approximately 9.8 years.

The complete life cycle of this species is illustrated in the figure below:

Plate 4. Life Cycle of Bathydoris hodgsoni (Specimens and Clutches Collected in the Weddell Sea) A: Medium-sized adult specimen. B: The same specimen alongside its clutch containing two eggs. Note the relative size of the animal and the clutch compared to the centimeter ruler for scale. C: Spawn of two eggs, each containing visible juveniles. An artificially hatched juvenile is shown on the right. D: Juvenile recently hatched under artificial conditions. Photos by M. Ballesteros.

Figure 2. Bathydoris hodgsoni. A: Spawn consisting of three eggs. The egg on the left contains an undeveloped embryo, the central egg shows an embryo in the juvenile stage, and the egg on the right is empty following the juvenile’s hatching. B: Lateral view of an egg. C: Newly hatched juvenile. D: Close-up of the dorsal tubercles of the newly hatched juvenile, highlighting the presence of secondary tubercles. E: Anal papilla surrounded by six gill leaves. F: Detail of the foot’s spicule reticulum and granulations. G: Ventral view of the newly hatched juvenile. Original illustrations by M. Ballesteros.

 

Discussion and Conclusions

The biology of these two remarkable Antarctic nudibranch species shares notable traits, including direct development without a larval phase, prolonged embryonic development, and, in the case of Bathydoris hodgsoni, the substantial size that adults can achieve. Both species are believed to have exceptionally long lifespans, likely linked to their low metabolic rates in the cold, stable waters of the Antarctic. Characteristics such as gigantism, slow growth, and extended embryonic development have been observed in various Antarctic marine invertebrates, including pycnogonids, sponges, isopods, amphipod crustaceans, and echinoderms, among others (Clarke, 1983; Moran & Woods, 2012). Another notable adaptation in Antarctic marine invertebrates is the ability of many starfish species to incubate their eggs, a phenomenon that underscores the evolutionary response to their cold, oxygen-rich environment.

Existing research suggests that Antarctic marine invertebrates exhibit extraordinary longevity, often far exceeding their temperate-water relatives. For instance, shelled gastropods in Antarctica are reported to live up to 30 times longer than closely related species in warmer waters (Pearse et al., 1991; Hain & Arnaud, 1992). Recent findings by Moran et al. (2019) confirm that the buccinoid gastropod Antarctodomus thielei, which also has direct development, requires over eight years for its eggs to develop and hatch. These findings highlight the slow pace of life and reproduction in Antarctic species. Future studies of other Antarctic marine invertebrates are likely to reveal further extraordinary insights into their reproductive strategies and life histories.

 

Acknowledgements

I would like to express my gratitude to Javier Cristobo and Jose Antonio Moya for their invaluable companionship and support during countless hours of diving and laboratory work on King George Island during the 2006 campaign. I also extend my thanks to Ana Ramos, the leader of the BENTART 2003 campaign, and all other team members who assisted in sample collection. Special thanks go to Conxita Àvila for her leadership during the ECOQUIM 2003–2004 campaign aboard the R.V. Polarstern, and to Wolf Arntz for his leadership and the crew of the R.V. Polarstern for their invaluable support during our research.

 

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